Introduction
The National Action Plan for Combating Antibiotic-Resistant Bacteria Progress Report: Year 5 highlights the importance of strengthening surveillance efforts via optimizing, expanding, and coordinating existing surveillance systems, like the Antimicrobial Resistance Laboratory Network (ARLN). 1,2 Understanding barriers and opportunities to improve multi-drug resistant organism (MDRO) reporting is paramount to addressing antibiotic resistance. Literature describing and evaluating the MDRO surveillance state is limited.
MDRO reporting is mandatory in Tennessee (Supplementary Figure 2). Laboratory results are submitted by electronic laboratory reporting, fax, or mail. Culture isolates should be sent within 3 days of detection to the regional ARLN laboratory in Nashville, Tennessee. This project aimed to describe MDRO reporting variability across Tennessee medical facilities and to identify opportunities to improve MDRO surveillance. We hypothesized that MDRO isolate submission times would vary by laboratory type (on-site versus reference), location, isolate source, MDRO, and temporal relationship to the COVID-19 pandemic.
Methods
This retrospective cohort study utilized pre-existing ARLN MDRO reporting database facility and patient data. After MDRO identification in Tennessee, reporting is a multi-step process involving facilities, laboratories, infection preventionists, and public health professionals.
Data collection
MDROs were defined as carbapenem-resistant Enterobacterales, carbapenem-resistant Acinetobacter baumannii, carbapenem-resistant Pseudomonas aeruginosa (CRPA), and Candida auris. Data were extracted from the southeast regional ARLN for 2018–2022 to ensure data completeness and availability and inclusion of time before and during the COVID-19 pandemic.
Isolates obtained for clinical purposes were included. ARLN personnel reviewed and decided whether wound and sputum cultures were clinical or surveillance specimens. Rectal, axillary, and groin isolates were considered surveillance specimens. All surveillance specimens were excluded.
Statistical analysis
Facility type (microbiology laboratory services on-site versus reference), MDRO, laboratory reporting region (East, Middle, West α ) based on laboratory zip code, temporal relationship to the COVID-19 pandemic, and specimen type were included. If a reference laboratory served multiple regions or a location could not be determined, the region was categorized as “no identified location.” Isolate reporting times were compared before and after Tennessee declared a State of Emergency for the COVID-19 pandemic on 3/2/2020.
Each MDRO isolate’s reporting time was categorized as fast (1–10 days), slow (11–-20 days), or delayed (21–100 days). Isolates reported as ≤0 or ≥100 days, likely representing data entry errors were excluded. Differences in number of isolates for each reporting time by groups were assessed using Pearson’s chi-square test (Microsoft Excel). Mean reporting times were analyzed using one-way analysis of variance with Tukey’s test (SAS 9.4).
Results
Of 9,569 MDRO clinical isolates included, 47 (0.5%) isolates were excluded for reporting times ≤0 or ≥100 days. Isolate reporting time designations (fast, slow, delayed) differed significantly for all variables (Supplementary Table 1). There was no difference in mean reporting times by facility type (P = 0.06). CRPA was reported faster than other MDROs (P < 0.01). Specimens from West Tennessee (P < 0.01), specimens reported after Tennessee’s COVID-19 state of emergency was declared, and blood cultures had significantly slower reporting times (P < 0.01, Figure 1).
The average time to report based on facility type, MDRO type, reporting region, pre- and during COVID-19, and specimen type.
Discussion
Rising MDRO numbers underscore the need for effective surveillance efforts. 1,2 These data suggest there are likely facility-level barriers and opportunities that, if addressed, could result in more consistent, reliable MDRO surveillance across Tennessee.
Reporting delays were associated with specific variables. Reporting delays in West Tennessee isolates may be due to the distance from the ARLN in Nashville, Tennessee, or potentially from resource disparities. Memphis, the largest city in West Tennessee, is >200 miles from Nashville. The lower number of isolates submitted from this region also suggests a potential lack of MDRO reporting, possibly due to a lower MRDO burden or possibly from other unidentified, unique barriers. Blood culture processing using traditional culture methods requires more time than other specimen types, and availability and utilization of rapid diagnostic capabilities to identify MDROs vary widely. Reference van Belkum, Durand and Peyret3
Finally, declaration of a COVID-19 State of Emergency disrupted laboratory workflow to varying degrees depending on local laboratory resiliency and capacity. Reference Lenert and Sundwall4 Delayed MDRO reporting impairs public health response in identifying and addressing geographical and temporal changes in MDRO prevalence, disease trends, and outbreak investigations.
Interestingly, despite expected additional time required to transport and process reference laboratory specimens, reference laboratory use trended towards faster reporting, although the difference did not reach statistical significance. Potential driving factors not measured in this study include the type of hospital system, use of courier services, laboratory technology, facility-specific reporting protocols, and involvement of infection prevention and antimicrobial stewardship teams in the reporting process. Reference Chandrasekera, Lesho and Chukwuma5 Further investigation of laboratory and facility-specific factors is needed to thoroughly understand potential barriers.
This study had limitations. Identifying the network of reporting microbiology laboratories was challenging. Therefore, data might only partially represent differences in regional reporting for microbiology laboratories that serve multiple hospitals. Unreported MDROs might skew these data; however, given the large number of isolates included, it is unlikely these represent a significant portion of data. Finally, relationships and reporting structures among public health departments in the United States may not mirror Tennessee, limiting generalizability; however, given minimal existing data, this study provides a framework from which others can develop tools to evaluate other surveillance systems outside of Tennessee.
Conclusion
MDRO isolates without timely reporting prohibit meaningful infection prevention strategies and identification of highly interconnected facilities that may pose higher risk of MDRO transmission among healthcare facilities and the community. Reference Lee, Bartsch and Wong6–Reference Overhage, Grannis and McDonald10 Future work will use qualitative studies to evaluate laboratory-specific and system-wide communication, technology, and resource capacity to identify opportunities to improve MDRO surveillance.
Supplementary material
To view supplementary material for this article, please visit https://doi.org/10.1017/ice.2025.10212
Competing interests
Matthew Lokant, MD: Matthew Lokant is a member of the Society for Healthcare Epidemiology Publications subcommittee.
Christopher Wilson, MD, MPH: No sources of financial support to disclose.
Thomas R. Talbot, MD, MPH: Member, Board of Directors, OmniSolve
Priscilla Pineda, MPH: No sources of financial support to disclose.
Erin Hitchingham, MPH: No sources of financial support to disclose.
Melphine Harriott, PhD: No sources of financial support to disclose.
Raquel Villegas, PhD, MS: No sources of financial support to disclose.
Kaleb Wolfe, MD: No sources of financial support to disclose.
Milner Staub, MD, MPH: Milner Staub works for Veteran Affairs; however, the views and opinions included in this manuscript do not necessarily represent those of the US Government or the Department of Veteran Affairs. Milner Staub is a member of the Society for Healthcare Epidemiology Research subcommittee.
